183
Views
5
CrossRef citations to date
0
Altmetric
Original Investigation

Effects of low-dose alcohol exposure in adolescence on subsequent alcohol drinking in adulthood in a rat model of depression

, , ORCID Icon, & ORCID Icon
Pages 757-769 | Received 29 Sep 2020, Accepted 26 Feb 2021, Published online: 23 Apr 2021

References

  • Acevedo MB, Nizhnikov ME, Spear NE, Molina JC, Pautassi RM. 2013. Ethanol-induced locomotor activity in adolescent rats and the relationship with ethanol-induced conditioned place preference and conditioned taste aversion. Dev Psychobiol. 55:429–442.
  • Alaux-Cantin S, Warnault V, Legastelois R, Botia B, Pierrefiche O, Vilpoux C, et al. 2013. Alcohol intoxications during adolescence increase motivation for alcohol in adult rats and induce neuroadaptations in the nucleus accumbens. Neuropharmacology. 67:521–531.
  • Amchova P, Kucerova J, Giugliano V, Babinska Z, Zanda MT, Scherma M, et al. 2014. Enhanced self-administration of the CB1 receptor agonist WIN55,212-2 in olfactory bulbectomized rats: evaluation of possible serotonergic and dopaminergic underlying mechanisms. Front Pharmacol. 5:44.
  • Amodeo LR, Kneiber D, Wills DN, Ehlers CL. 2017. Alcohol drinking during adolescence increases consumptive responses to alcohol in adulthood in Wistar rats. Alcohol Fayettev N. 59:43–51.
  • Anderson RI, Varlinskaya EI, Spear LP. 2010. Ethanol-induced conditioned taste aversion in male sprague-dawley rats: impact of age and stress. Alcohol Clin Exp Res. 34:2106–2115.
  • Ayers-Ringler JR, Jia Y-F, Qiu Y-Y, Choi D-S. 2016. Role of astrocytic glutamate transporter in alcohol use disorder. World J Psychiatry. 6:31–42.
  • Babinska Z, Ruda-Kucerova J. 2017. Differential characteristics of ketamine self-administration in the olfactory bulbectomy model of depression in male rats. Exp Clin Psychopharmacol. 25:84–93.
  • Bartlett MS, Fowler RH. 1937. Properties of sufficiency and statistical tests. Proc R Soc Lond Ser Math Phys Sci. 160:268–282.
  • Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. J Stat Softw. 67:1–48.
  • Bazargan-Hejazi S, Bazargan M, Gaines T, Jemanez M. 2008. Alcohol misuse and report of recent depressive symptoms among ED patients. Am J Emerg Med. 26:537–544.
  • Berridge KC, Robinson TE. 2016. Liking, wanting, and the incentive-sensitization theory of addiction. Am Psychol. 71:670–679.
  • Boisgontier MP, Cheval B. 2016. The anova to mixed model transition. Neurosci Biobehav Rev. 68:1004–1005.
  • Bokor G, Anderson PD. 2014. Ketamine: an update on its abuse. J Pharm Pract. 27:582–586.
  • Boutros N, Semenova S, Liu W, Crews FT, Markou A. 2014. Adolescent intermittent ethanol exposure is associated with increased risky choice and decreased dopaminergic and cholinergic neuron markers in adult rats. Int J Neuropsychopharmacol. 18:pyu003.
  • Bozymski KM, Crouse EL, Titus-Lay EN, Ott CA, Nofziger JL, Kirkwood CK. 2019. Esketamine: a novel option for treatment-resistant depression. Ann Pharmacother. 54:567–576.
  • Broadwater M, Varlinskaya EI, Spear LP. 2013. Effects of voluntary access to sweetened ethanol during adolescence on intake in adulthood. Alcohol Clin Exp Res. 37:1048–1055.
  • Brook DW, Brook JS, Zhang C, Cohen P, Whiteman M. 2002. Drug use and the risk of major depressive disorder, alcohol dependence, and substance use disorders. Arch Gen Psychiatry. 59:1039–1044.
  • Cannady R, Fisher KR, Durant B, Besheer J, Hodge CW. 2013. Enhanced AMPA receptor activity increases operant alcohol self-administration and cue-induced reinstatement. Addict Biol. 18:54–65.
  • Cano-Cebrián MJ, Zornoza-Sabina T, Guerri C, Polache A, Granero L. 2003. Local acamprosate modulates dopamine release in the rat nucleus accumbens through NMDA receptors: an in vivo microdialysis study. Naunyn Schmiedebergs Arch Pharmacol. 367:119–125.
  • Canuso CM, Singh JB, Fedgchin M, Alphs L, Lane R, Lim P, et al. 2018. Efficacy and safety of intranasal esketamine for the rapid reduction of symptoms of depression and suicidality in patients at imminent risk for suicide: results of a double-blind, randomized, placebo-controlled study. Am J Psychiatry. 175:620–630.
  • Carnicella S, Ron D, Barak S. 2014. Intermittent ethanol access schedule in rats as a preclinical model of alcohol abuse. Alcohol Fayettev N. 48:243–252.
  • Carnicella S, Yowell QV, Ron D. 2011. Regulation of operant oral ethanol self-administration: a dose-response curve study in rats. Alcohol Clin Exp Res. 35:116–125.
  • Chwedorowicz R, Skarżyński H, Pucek W, Studziński T. 2017. Neurophysiological maturation in adolescence - vulnerability and counteracting addiction to alcohol. Ann Agric Environ Med AAEM. 24:19–25.
  • Cofresí RU, Bartholow BD, Piasecki TM. 2019. Evidence for incentive salience sensitization as a pathway to alcohol use disorder. Neurosci Biobehav Rev. 107:897–926.
  • Crews FT, Vetreno RP, Broadwater MA, Robinson DL. 2016. Adolescent alcohol exposure persistently impacts adult neurobiology and behavior. Pharmacol Rev. 68:1074–1109.
  • Czachowski CL, Delory MJ, Pope JD. 2012. Behavioral and neurotransmitter specific roles for the ventral tegmental area in reinforcer-seeking and intake. Alcohol Clin Exp Res. 36:1659–1668.
  • de Graaf R, Bijl RV, Spijker J, Beekman ATF, Vollebergh W, A M. 2003. Temporal sequencing of lifetime mood disorders in relation to comorbid anxiety and substance use disorders-findings from the Netherlands Mental Health Survey and Incidence Study. Soc Psychiatry Psychiatr Epidemiol. 38:1–11.
  • Ding ZM, Katner SN, Rodd ZA, Truitt W, Hauser SR, Deehan GA, et al. 2012. Repeated exposure of the posterior ventral tegmental area to nicotine increases the sensitivity of local dopamine neurons to the stimulating effects of ethanol. Alcohol Fayettev N. 46:217–223.
  • Doremus-Fitzwater TL, Spear LP. 2016. Reward-centricity and attenuated aversions: an adolescent phenotype emerging from studies in laboratory animals. Neurosci Biobehav Rev. 70:121–134.
  • Frankowska M, Jastrzębska J, Nowak E, Białko M, Przegaliński E, Filip M. 2014. The effects of N-acetylcysteine on cocaine reward and seeking behaviors in a rat model of depression. Behav Brain Res. 266:108–118.
  • García-Burgos D, González F, Manrique T, Gallo M. 2009. Patterns of ethanol intake in preadolescent, adolescent, and adult Wistar rats under acquisition, maintenance, and relapse-like conditions. Alcohol Clin Exp Res. 33:722–728.
  • Getachew B, Tizabi Y. 2019. Both ketamine and NBQX attenuate alcohol-withdrawal induced depression in male rats. J Drug Alcohol Res. 8:236069.
  • Gómez-Coronado N, Sethi R, Bortolasci CC, Arancini L, Berk M, Dodd S. 2018. A review of the neurobiological underpinning of comorbid substance use and mood disorders. J Affect Disord. 241:388–401.
  • Gong X, Chen Y, Chang J, Huang Y, Cai M, Zhang M. 2018. Environmental enrichment reduces adolescent anxiety- and depression-like behaviors of rats subjected to infant nerve injury. J Neuroinflammation. 15:262.
  • Grant BF, Harford TC. 1995. Comorbidity between DSM-IV alcohol use disorders and major depression: results of a national survey. Drug Alcohol Depend. 39:197–206.
  • Grecksch G, Becker A. 2015. Alterations of reward mechanisms in bulbectomised rats. Behav Brain Res. 286:271–277.
  • Gueorguieva R, Krystal JH. 2004. Move over ANOVA: progress in analyzing repeated-measures data and its reflection in papers published in the Archives of General Psychiatry. Arch Gen Psychiatry. 61:310–317.
  • Hasin D. 2003. Classification of alcohol use disorders. Alcohol Res Health. 27:5–17.
  • Hasin DS, O’Brien CP, Auriacombe M, Borges G, Bucholz K, Budney A, et al. 2013. DSM-5 criteria for substance use disorders: recommendations and rationale. Am J Psychiatry. 170:834–851.
  • Holmes PV, Masini CV, Primeaux SD, Garrett JL, Zellner A, Stogner KS, et al. 2002. Intravenous self-administration of amphetamine is increased in a rat model of depression. Synapse. 46:4–10.
  • Huang MC, Lin SK. 2020. Ketamine abuse: past and present. In: Hashimoto K, Ide S, Ikeda K, editors. Ketamine: from abused drug to rapid-acting antidepressant. Singapore: Springer; p. 1–14.
  • Jordan CJ, Andersen SL. 2017. Sensitive periods of substance abuse: early risk for the transition to dependence. Dev Cogn Neurosci. 25:29–44.
  • Kalivas PW. 2000. A role for glutamate transmission in addiction to psychostimulants. Addict Biol. 5:325–329.
  • Katkov YA, Otmakhova NA, Gurevich EV, Nesterova IV, Bobkova NV. 1994. Antidepressants suppress bulbectomy-induced augmentation of voluntary alcohol consumption in C57B1/6j but not in DBA/2j mice. Physiol Behav. 56:501–509.
  • Kaur U, Pathak BK, Singh A, Chakrabarti SS. 2019. Esketamine: a glimmer of hope in treatment-resistant depression. Eur Arch Psychiatry Clin Neurosci. 271:417–429.
  • Kelly JP, Wrynn AS, Leonard BE. 1997. The olfactory bulbectomized rat as a model of depression: an update. Pharmacol Ther. 74:299–316.
  • Kucerova J, Pistovcakova J, Vrskova D, Dusek L, Sulcova A. 2012. The effects of methamphetamine self-administration on behavioural sensitization in the olfactory bulbectomy rat model of depression. Int J Neuropsychopharmacol. 15:1503–1511.
  • Liu W, Crews FT. 2017. Persistent decreases in adult subventricular and hippocampal neurogenesis following adolescent intermittent ethanol exposure. Front Behav Neurosci. 11:151.
  • Lo Iacono L, Carola V. 2018. The impact of adolescent stress experiences on neurobiological development. Semin Cell Dev Biol. 77:93–103.
  • Lorenz RC, Gleich T, Beck A, Pöhland L, Raufelder D, Sommer W, et al. 2014. Reward anticipation in the adolescent and aging brain. Hum Brain Mapp. 35:5153–5165.
  • Marco EM, Ballesta JA, Irala C, Hernández M-D, Serrano ME, Mela V, et al. 2017. Sex-dependent influence of chronic mild stress (CMS) on voluntary alcohol consumption; study of neurobiological consequences. Pharmacol Biochem Behav. 152:68–80.
  • Márquez J, Campos-Sandoval JA, Peñalver A, Matés JM, Segura JA, Blanco E, et al. 2017. Glutamate and brain glutaminases in drug addiction. Neurochem Res. 42:846–857.
  • McHugh RK, Weiss RD. 2019. Alcohol use disorder and depressive disorders. Alcohol Res. 40:arcr.v40.1.01.
  • Mendiburu FD. 2020. Agricolae: statistical procedures for agricultural research. https://CRAN.R-project.org/package=agricolae
  • Nelson TE, Ur CL, Gruol DL. 2005. Chronic intermittent ethanol exposure enhances NMDA-receptor-mediated synaptic responses and NMDA receptor expression in hippocampal CA1 region. Brain Res. 1048:69–79.
  • Nona CN, Hendershot CS, Lê AD. 2018. Behavioural sensitization to alcohol: bridging the gap between preclinical research and human models. Pharmacol Biochem Behav. 173:15–26.
  • Ohgi Y, Futamura T, Hashimoto K. 2015. Glutamate signaling in synaptogenesis and NMDA receptors as potential therapeutic targets for psychiatric disorders. Curr Mol Med. 15:206–221.
  • Olloquequi J, Cornejo-Córdova E, Verdaguer E, Soriano FX, Binvignat O, Auladell C, et al. 2018. Excitotoxicity in the pathogenesis of neurological and psychiatric disorders: therapeutic implications. J Psychopharmacol Oxf Engl. 32:265–275.
  • Pandey SC, Sakharkar AJ, Tang L, Zhang H. 2015. Potential role of adolescent alcohol exposure-induced amygdaloid histone modifications in anxiety and alcohol intake during adulthood. Neurobiol Dis. 82:607–619.
  • Pautassi RM, Godoy JC, Molina JC. 2015. Adolescent rats are resistant to the development of ethanol-induced chronic tolerance and ethanol-induced conditioned aversion. Pharmacol Biochem Behav. 138:58–69.
  • R Core Team. 2020. R: a language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing. https://www.R-project.org/
  • Rammes G, Mahal B, Putzke J, Parsons C, Spielmanns P, Pestel E, et al. 2001. The anti-craving compound acamprosate acts as a weak NMDA-receptor antagonist, but modulates NMDA-receptor subunit expression similar to memantine and MK-801. Neuropharmacology. 40:749–760.
  • Rao PSS, Bell RL, Engleman EA, Sari Y. 2015. Targeting glutamate uptake to treat alcohol use disorders. Front Neurosci. 9:144.
  • Rezvani AH, Levin ED, Cauley M, Getachew B, Tizabi Y. 2017. Ketamine differentially attenuates alcohol intake in male versus female alcohol preferring (P) rats. J Drug Alcohol Res. 6:236030.
  • Robinson TE, Berridge KC. 1993. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev. 18:247–291.
  • Ruda-Kucerova J, Amchova P, Babinska Z, Dusek L, Micale V, Sulcova A. 2015. Sex differences in the reinstatement of methamphetamine seeking after forced abstinence in Sprague-Dawley rats. Front Psychiatry. 6:91.
  • Ruda-Kucerova J, Amchova P, Havlickova T, Jerabek P, Babinska Z, Kacer P, et al. 2015. Reward related neurotransmitter changes in a model of depression: an in vivo microdialysis study. World J Biol Psychiatry. 16:521–535.
  • Ruda-Kucerova J, Babinska Z, Amchova P, Stark T, Drago F, Sulcova A, et al. 2017. Reactivity to addictive drugs in the methylazoxymethanol (MAM) model of schizophrenia in male and female rats. World J Biol Psychiatry. 18:129–142.
  • Ruda-Kucerova J, Babinska Z, Luptak M, Getachew B, Tizabi Y. 2018. Both ketamine and NBQX attenuate alcohol drinking in male Wistar rats. Neurosci Lett. 666:175–180.
  • Ruda-Kucerova J, Babinska Z, Stark T, Micale V. 2017. Suppression of methamphetamine self-administration by ketamine pre-treatment is absent in the methylazoxymethanol (MAM) rat model of schizophrenia. Neurotox Res. 32:121–133.
  • Saalfield J, Spear L. 2015. Consequences of repeated ethanol exposure during early or late adolescence on conditioned taste aversions in rats. Dev Cogn Neurosci. 16:174–182.
  • Scofield MD, Heinsbroek JA, Gipson CD, Kupchik YM, Spencer S, Smith ACW, et al. 2016. The nucleus accumbens: mechanisms of addiction across drug classes reflect the importance of glutamate homeostasis. Pharmacol Rev. 68:816–871.
  • Seong HH, Park JM, Kim YJ. 2018. Antidepressive effects of environmental enrichment in chronic stress-induced depression in rats. Biol Res Nurs. 20:40–48.
  • Siegmund S, Vengeliene V, Singer MV, Spanagel R. 2005. Influence of age at drinking onset on long-term ethanol self-administration with deprivation and stress phases. Alcohol Clin Exp Res. 29:1139–1145.
  • Šlamberová R, Rudá-Kučerová J, Babinská Z, Ševčíková M. 2017. Olfactory bulbectomy in methamphetamine-treated rat mothers induces impairment in somatic and functional development of their offspring. Physiol Res. 66:S469–S479.
  • Song C, Leonard BE. 2005. The olfactory bulbectomised rat as a model of depression. Neurosci Biobehav Rev. 29:627–647.
  • Soyka M, Müller CA. 2017. Pharmacotherapy of alcoholism - an update on approved and off-label medications. Expert Opin Pharmacother. 18:1187–1199.
  • Spear LP. 2018. Effects of adolescent alcohol consumption on the brain and behaviour. Nat Rev Neurosci. 19:197–214.
  • Stephens DN, Brown G. 1999. Disruption of operant oral self-administration of ethanol, sucrose, and saccharin by the AMPA/kainate antagonist, NBQX, but not the AMPA antagonist, GYKI 52466. Alcohol Clin Exp Res. 23:1914–1920.
  • Swift RM, Aston ER. 2015. Pharmacotherapy for alcohol use disorder: current and emerging therapies. Harv Rev Psychiatry. 23:122–133.
  • Thibodeau M, Pickering GJ. 2019. The role of taste in alcohol preference, consumption and risk behavior. Crit Rev Food Sci Nutr. 59:676–692.
  • Thompson A, Ashcroft DM, Owens L, van Staa TP, Pirmohamed M. 2017. Drug therapy for alcohol dependence in primary care in the UK: A Clinical Practice Research Datalink study. PloS One 12:e0173272.
  • Tibboel H, De Houwer J, Van Bockstaele B. 2015. Implicit measures of “wanting” and “liking” in humans. Neurosci Biobehav Rev. 57:350–364.
  • Tizabi Y. 2007. Nicotine and nicotinic system in hypoglutamatergic models of schizophrenia. Neurotox Res. 12:233–246.
  • Tizabi Y, Getachew B, Ferguson CL, Csoka AB, Thompson KM, Gomez-Paz A, Ruda-Kucerova J, Taylor RE. 2018. Low vs. high alcohol: central benefits vs. detriments. Neurotox Res. 34:860–869.
  • Tomek SE, Lacrosse AL, Nemirovsky NE, Olive MF. 2013. NMDA receptor modulators in the treatment of drug addiction. Pharmaceuticals (Basel). 6:251–268.
  • Towner TT, Varlinskaya EI. 2020. Adolescent ethanol exposure: anxiety-like behavioral alterations, ethanol intake, and sensitivity. Front Behav Neurosci. 14:45.
  • Turner S, Mota N, Bolton J, Sareen J. 2018. Self-medication with alcohol or drugs for mood and anxiety disorders: a narrative review of the epidemiological literature. Depress Anxiety. 35:851–860.
  • Vázquez-León P, Martínez-Mota L, Quevedo-Corona L, Miranda-Páez A. 2017. Isolation stress and chronic mild stress induced immobility in the defensive burying behavior and a transient increased ethanol intake in Wistar rats. Alcohol. 63:43–51.
  • Vetter CS, Doremus-Fitzwater TL, Spear LP. 2007. Time course of elevated ethanol intake in adolescent relative to adult rats under continuous, voluntary-access conditions. Alcohol Clin Exp Res. 31:1159–1168.
  • Vieyra-Reyes P, Mineur YS, Picciotto MR, Túnez I, Vidaltamayo R, Drucker-Colín R. 2008. Antidepressant-like effects of nicotine and transcranial magnetic stimulation in the olfactory bulbectomy rat model of depression. Brain Res Bull. 77:13–18.
  • Wilkinson ST, Sanacora G. 2019. A new generation of antidepressants: an update on the pharmaceutical pipeline for novel and rapid-acting therapeutics in mood disorders based on glutamate/GABA neurotransmitter systems. Drug Discov Today. 24:606–615.
  • Wille-Bille A, de Olmos S, Marengo L, Chiner F, Pautassi RM. 2017. Long-term ethanol self-administration induces ΔFosB in male and female adolescent, but not in adult, Wistar rats. Prog Neuropsychopharmacol Biol Psychiatry. 74:15–30.
  • Williams KL, Nickel MM, Bielak JT. 2018. Oral binge-like ethanol pre-exposure during juvenile/adolescent period attenuates ethanol-induced conditioned place aversion in rats. Alcohol Alcohol. 53:518–525.
  • World Health Organization. 2017. Depression and other common mental disorders: global Health Estimates. Geneva.
  • World Health Organization 2018. Global status report on alcohol and health. 2018th ed. Geneva.
  • Yandell B. 1997. Practical data analysis for designed experiments. Boston (MA): Springer.
  • Yuan M, Cross SJ, Loughlin SE, Leslie FM. 2015. Nicotine and the adolescent brain. J Physiol. 593:3397–3412.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.